HPAIV outbreak triggers short-term colony connectivity in a seabird metapopulation.

Disease outbreaks can drastically disturb the environment of surviving animals, but the behavioural, ecological, and epidemiological consequences of disease-driven disturbance are poorly understood. Here, we show that an outbreak of High Pathogenicity Avian Influenza Virus (HPAIV) coincided with unprecedented short-term behavioural changes in Northern gannets (Morus bassanus). Breeding gannets show characteristically strong fidelity to their nest sites and foraging areas (2015-2019; n = 120), but during the 2022 HPAIV outbreak, GPS-tagged gannets instigated long-distance movements beyond well-documented previous ranges and the first ever recorded visits of GPS-tagged adults to other gannet breeding colonies. Our findings suggest that the HPAIV outbreak triggered changes in space use patterns of exposed individuals that amplified the epidemiological connectivity among colonies and may generate super-spreader events that accelerate disease transmission across the metapopulation. Such self-propagating transmission from and towards high density animal aggregations may explain the unexpectedly rapid pan-European spread of HPAIV in the gannet.

Haemoproteus parasites and passerines: the effect of local generalists on inferences of host-parasite co-phylogeny in the British Isles.

Host­parasite associations provide a benchmark for investigating evolutionary arms races and antagonistic coevolution. However, potential ecological mechanisms underlying such associations are difficult to unravel. In particular, local adaptations of hosts and/or parasites may hamper reliable inferences of host­parasite relationships and the specialist­generalist definitions of parasite lineages, making it problematic to understand such relationships on a global scale. Phylogenetic methods were used to investigate co-phylogenetic patterns between vector-borne parasites of the genus Haemoproteus and their passeriform hosts, to infer the ecological interactions of parasites and hosts that may have driven the evolution of both groups in a local geographic domain. As several Haemoproteus lineages were only detected once, and given the occurrence of a single extreme generalist, the effect of removing individual lineages on the co-phylogeny pattern was tested. When all lineages were included, and when all singly detected lineages were removed, there was no convincing evidence for host­parasite co-phylogeny. However, when only the generalist lineage was removed, strong support for co-phylogeny was indicated, and ecological interactions could be successfully inferred. This study exemplifies the importance of identifying locally abundant lineages when sampling host­parasite systems, to provide reliable insights into the precise mechanisms underlying host­parasite interactions.

Assessing rates of parasite coinfection and spatiotemporal strain variation via metabarcoding: Insights for the conservation of European turtle doves Streptopelia turtur.

Understanding the frequency, spatiotemporal dynamics and impacts of parasite coinfections is fundamental to developing control measures and predicting disease impacts. The European turtle dove (Streptopelia turtur) is one of Europe's most threatened bird species. High prevalence of infection by the protozoan parasite Trichomonas gallinae has previously been identified, but the role of this and other coinfecting parasites in turtle dove declines remains unclear. Using a high-throughput sequencing approach, we identified seven strains of T. gallinae, including two novel strains, from ITS1/5.8S/ITS2 ribosomal sequences in turtle doves on breeding and wintering grounds, with further intrastrain variation and four novel subtypes revealed by the iron-hydrogenase gene. High spatiotemporal turnover was observed in T. gallinae strain composition, and infection was prevalent in all populations (89%-100%). Coinfection by multiple Trichomonas strains was rarer than expected (1% observed compared to 38.6% expected), suggesting either within-host competition, or high mortality of coinfected individuals. In contrast, coinfection by multiple haemosporidians was common (43%), as was coinfection by haemosporidians and T. gallinae (90%), with positive associations between strains of T. gallinae and Leucocytozoon suggesting a mechanism such as parasite-induced immune modulation. We found no evidence for negative associations between coinfections and host body condition. We suggest that longitudinal studies involving the recapture and investigation of infection status of individuals over their lifespan are crucial to understand the epidemiology of coinfections in natural populations.

Risks to different populations and age classes of gannets from impacts of offshore wind farms in the southern North Sea.

The southern North Sea holds the world's highest concentration of offshore wind farms (OWFs). Northern gannets (Morus bassanus), a species considered at high risk from OWF impacts, show a strong seasonal peak there in November, but it is unclear which populations and age classes are most at risk of collision with wind turbines. We tagged adult and juvenile gannets at the world's largest colony (Bass Rock) and reviewed two sources of survey data for different age classes to study their movements through southern North Sea waters. Tracked birds showed peak numbers in the southern North Sea in mid-October, with much smaller numbers there during November. Adults were distributed throughout the area, including waters close to OWFs, whereas juveniles were confined to the coast. Survey data indicated high proportions of immature gannets in southern North Sea waters, suggesting higher collision risk than for adults. Gannets present in November may be predominantly from colonies further north than Bass Rock.

Tropical land-use change alters trait-based community assembly rules for dung beetles and birds.

Tropical rainforest disturbance and conversion are critical drivers of biodiversity loss. A key knowledge gap is understanding the impacts of habitat modification on mechanisms of community assembly, which are predicted to respond differently between taxa and across spatial scales. We use a null model approach to detect trait assembly of species at local- and landscape-scales, and then subdivide communities with different habitat associations and foraging guilds to investigate whether the detection of assembly mechanisms varies between groups. We focus on two indicator taxa, dung beetles and birds, across a disturbance gradient of primary rainforest, selectively logged rainforest, and oil palm plantations in Borneo, Southeast Asia. Random community assembly was predominant for dung beetles across habitats, whereas trait convergence, indicative of environmental filtering, occurred across the disturbance gradient for birds. Assembly patterns at the two spatial scales were similar. Subdividing for habitat association and foraging guild revealed patterns hidden when focusing on the overall community. Dung beetle forest specialists and habitat generalists showed opposing assembly mechanisms in primary forest, community assembly of habitat generalists for both taxa differed with disturbance intensity, and insectivorous birds strongly influenced overall community assembly relative to other guilds. Our study reveals the sensitivity of community assembly mechanisms to anthropogenic disturbance via a shift in the relative contribution of stochastic and deterministic processes. This highlights the need for greater understanding of how habitat modification alters species interactions and the importance of incorporating species' traits within assessments.

Vulnerability of northern gannets to offshore wind farms; seasonal and sex-specific collision risk and demographic consequences.

There is a pressing need to quantify the risks of renewable energy developments such as offshore wind farms for protected populations. However, assessments are often based on incomplete data, or fail to consider variation in risk between sexes and at different times of year. We tracked northern gannets foraging from the world's largest colony (Bass Rock, Scotland) across five consecutive breeding seasons. We examine how seasonal and sex differences in behaviour affect the collision risk from planned and operational wind farms within their foraging range and assess the likely consequences for long-term population viability. Both sexes made shorter trips during chick-rearing than prior to chick-hatching, spent a greater proportion of time within wind farm sites and had an eight times greater potential collision risk during chick-rearing. Females made longer trips than males at both these times of year, flew higher and spent more time within wind farm sites, leading to three times greater collision risk for females. After accounting for the potential additional mortality from collisions, and assuming that the death of a parent also led to the loss of its offspring, the breeding population was projected to increase by 3.57% (95% CI: 2.16-5.15%) per year, compared with 6.56% (95% CI: 4.59-8.73%) in the absence of turbines, suggesting a negligible effect on population viability. However, additional mortality could result in greater immigration from neighbouring colonies, potentially affecting their viability and highlighting a need for research within a metapopulation framework to assess the impacts of offshore wind developments on vulnerable species across multiple connected sites.

Understanding the ontogeny of foraging behaviour: insights from combining marine predator bio-logging with satellite-derived oceanography in hidden Markov models.

The development of foraging strategies that enable juveniles to efficiently identify and exploit predictable habitat features is critical for survival and long-term fitness. In the marine environment, meso- and sub-mesoscale features such as oceanographic fronts offer a visible cue to enhanced foraging conditions, but how individuals learn to identify these features is a mystery. In this study, we investigate age-related differences in the fine-scale foraging behaviour of adult (aged ≥ 5 years) and immature (aged 2-4 years) northern gannets Morus bassanus Using high-resolution GPS-loggers, we reveal that adults have a much narrower foraging distribution than immature birds and much higher individual foraging site fidelity. By conditioning the transition probabilities of a hidden Markov model on satellite-derived measures of frontal activity, we then demonstrate that adults show a stronger response to frontal activity than immature birds, and are more likely to commence foraging behaviour as frontal intensity increases. Together, these results indicate that adult gannets are more proficient foragers than immatures, supporting the hypothesis that foraging specializations are learned during individual exploratory behaviour in early life. Such memory-based individual foraging strategies may also explain the extended period of immaturity observed in gannets and many other long-lived species.

Search and foraging behaviors from movement data: A comparison of methods.

Search behavior is often used as a proxy for foraging effort within studies of animal movement, despite it being only one part of the foraging process, which also includes prey capture. While methods for validating prey capture exist, many studies rely solely on behavioral annotation of animal movement data to identify search and infer prey capture attempts. However, the degree to which search correlates with prey capture is largely untested. This study applied seven behavioral annotation methods to identify search behavior from GPS tracks of northern gannets (Morus bassanus), and compared outputs to the occurrence of dives recorded by simultaneously deployed time-depth recorders. We tested how behavioral annotation methods vary in their ability to identify search behavior leading to dive events. There was considerable variation in the number of dives occurring within search areas across methods. Hidden Markov models proved to be the most successful, with 81% of all dives occurring within areas identified as search. k-Means clustering and first passage time had the highest rates of dives occurring outside identified search behavior. First passage time and hidden Markov models had the lowest rates of false positives, identifying fewer search areas with no dives. All behavioral annotation methods had advantages and drawbacks in terms of the complexity of analysis and ability to reflect prey capture events while minimizing the number of false positives and false negatives. We used these results, with consideration of analytical difficulty, to provide advice on the most appropriate methods for use where prey capture behavior is not available. This study highlights a need to critically assess and carefully choose a behavioral annotation method suitable for the research question being addressed, or resulting species management frameworks established.

Author Correction: Long-term carbon sink in Borneo's forests halted by drought and vulnerable to edges.

The original version of this Article contained an error in the third sentence of the abstract and incorrectly read "Here, using long-term plot monitoring records of up to half a century, we find that intact forests in Borneo gained 0.43 Mg C ha-1 year-1 (95% CI 0.14-0.72, mean period 1988-2010) above-ground live biomass", rather than the correct "Here, using long-term plot monitoring records of up to half a century, we find that intact forests in Borneo gained 0.43 Mg C ha-1 year-1 (95% CI 0.14-0.72, mean period 1988-2010) in above-ground live biomass carbon". This has now been corrected in both the PDF and HTML versions of the Article.

Long-term carbon sink in Borneo's forests halted by drought and vulnerable to edge effects.

Less than half of anthropogenic carbon dioxide emissions remain in the atmosphere. While carbon balance models imply large carbon uptake in tropical forests, direct on-the-ground observations are still lacking in Southeast Asia. Here, using long-term plot monitoring records of up to half a century, we find that intact forests in Borneo gained 0.43 Mg C ha-1 per year (95% CI 0.14-0.72, mean period 1988-2010) above-ground live biomass. These results closely match those from African and Amazonian plot networks, suggesting that the world's remaining intact tropical forests are now en masse out-of-equilibrium. Although both pan-tropical and long-term, the sink in remaining intact forests appears vulnerable to climate and land use changes. Across Borneo the 1997-1998 El Niño drought temporarily halted the carbon sink by increasing tree mortality, while fragmentation persistently offset the sink and turned many edge-affected forests into a carbon source to the atmosphere.

Effects of age and reproductive status on individual foraging site fidelity in a long-lived marine predator.

Individual foraging specializations, where individuals use a small component of the population niche width, are widespread in nature with important ecological and evolutionary implications. In long-lived animals, foraging ability develops with age, but we know little about the ontogeny of individuality in foraging. Here we use precision global positioning system (GPS) loggers to examine how individual foraging site fidelity (IFSF), a common component of foraging specialization, varies between breeders, failed breeders and immatures in a long-lived marine predator-the northern gannet Morus bassanus Breeders (aged 5+) showed strong IFSF: they had similar routes and were faithful to distal points during successive trips. However, centrally placed immatures (aged 2-3) were far more exploratory and lacked route or foraging site fidelity. Failed breeders were intermediate: some with strong fidelity, others being more exploratory. Individual foraging specializations were previously thought to arise as a function of heritable phenotypic differences or via social transmission. Our results instead suggest a third alternative-in long-lived species foraging sites are learned during exploratory behaviours early in life, which become canalized with age and experience, and refined where possible-the exploration-refinement foraging hypothesis. We speculate similar patterns may be present in other long-lived species and moreover that long periods of immaturity may be a consequence of such memory-based individual foraging strategies.

High prevalence of Trichomonas gallinae in wild columbids across western and southern Europe.

BACKGROUND: Avian trichomonosis is known as a widespread disease in columbids and passerines, and recent findings have highlighted the pathogenic character of some lineages found in wild birds. Trichomonosis can affect wild bird populations including endangered species, as has been shown for Mauritian pink pigeons Nesoenas mayeri in Mauritius and suggested for European turtle doves Streptopelia turtur in the UK. However, the disease trichomonosis is caused only by pathogenic lineages of the parasite Trichomonas gallinae. Therefore, understanding the prevalence and distribution of both potentially pathogenic and non-pathogenic T. gallinae lineages in turtle doves and other columbids across Europe is relevant to estimate the potential impact of the disease on a continental scale. RESULTS: We examined 281 samples from four wild columbid species for Trichomonas infection and determined the genetic lineages. The overall prevalence was 74%. There were significant differences between the species (P = 0.007). The highest prevalence was found in stock doves Columba oenas (86%, n = 79) followed by wood pigeons Columba palumbus (70%, n = 61) and turtle doves (67%, n = 65), while three of five collared doves Streptopelia decaocto (60%) were infected. We found seven different lineages, including four lineages present in columbids in the UK, one lineage already described from Spain and three new lineages, one of those found in a single turtle dove migrating through Italy and another one found in a breeding stock dove. Stock doves from Germany and collared doves from Malta were infected with a potentially pathogenic lineage (lineage A/B), which is known to cause lesions and mortality in columbids, raptors and finches. CONCLUSIONS: Generally, turtle doves showed high prevalence of Trichomonas infection. Furthermore, the potentially pathogenic lineage A/B (or genotype B according to previous literature) was found in a recovering stock dove population. Both findings are worrying for these columbid species due to the occasional epidemic character of trichomonosis, which can have severe negative effects on populations.

The impact of logging roads on dung beetle assemblages in a tropical rainforest reserve.

The demand for timber products is facilitating the degradation and opening up of large areas of intact habitats rich in biodiversity. Logging creates an extensive network of access roads within the forest, yet these are commonly ignored or excluded when assessing impacts of logging on forest biodiversity. Here we determine the impact of these roads on the overall condition of selectively logged forests in Borneo, Southeast Asia. Focusing on dung beetles along > 40 km logging roads we determine: (i) the magnitude and extent of edge effects alongside logging roads; (ii) whether vegetation characteristics can explain patterns in dung beetle communities, and; (iii) how the inclusion of road edge forest impacts dung beetle assemblages within the overall logged landscape. We found that while vegetation structure was significantly affected up to 34 m from the road edge, impacts on dung beetle communities penetrated much further and were discernible up to 170 m into the forest interior. We found larger species and particularly tunnelling species responded more than other functional groups which were also influenced by micro-habitat variation. We provide important new insights into the long-term ecological impacts of tropical logging. We also support calls for improved logging road design both during and after timber extraction to conserve more effectively biodiversity in production forests, for instance, by considering the minimum volume of timber, per unit length of logging road needed to justify road construction. In particular, we suggest that governments and certification bodies need to highlight more clearly the biodiversity and environmental impacts of logging roads.

High rates of infection by blood parasites during the nestling phase in UK Columbids with notes on ecological associations.

Studies of blood parasite infection in nestling birds rarely find a high prevalence of infection. This is likely due to a combination of short nestling periods (limiting the age at which nestlings can be sampled) and long parasite prepatent periods before gametocytes can be detected in peripheral blood. Here we examine rates of blood parasite infection in nestlings from three Columbid species in the UK. We use this system to address two key hypotheses in the epidemiology of avian haemoparasites: first, that nestlings in open nests have a higher prevalence of infection; and second, that nestlings sampled at 14 days old have a higher apparent infection rate than those sampled at 7 days old. Open-nesting individuals had a 54% infection rate compared with 25% for box-nesters, probably due to an increased exposure of open-nesting species to dipteran vectors. Nestlings sampled at 14 days had a 68% infection rate compared with 32% in nestlings sampled at 7 days, suggesting that rates of infection in the nest are high. Further work should examine nestlings post-fledging to identify rates of successful parasite infection (as opposed to abortive development within a dead-end host) as well as impacts on host post-fledging survival and behaviour.

Anthropogenically-Mediated Density Dependence in a Declining Farmland Bird.

Land management intrinsically influences the distribution of animals and can consequently alter the potential for density-dependent processes to act within populations. For declining species, high densities of breeding territories are typically considered to represent productive populations. However, as density-dependent effects of food limitation or predator pressure may occur (especially when species are dependent upon separate nesting and foraging habitats), high territory density may limit per-capita productivity. Here, we use a declining but widespread European farmland bird, the yellowhammer Emberiza citrinella L., as a model system to test whether higher territory densities result in lower fledging success, parental provisioning rates or nestling growth rates compared to lower densities. Organic landscapes held higher territory densities, but nests on organic farms fledged fewer nestlings, translating to a 5 times higher rate of population shrinkage on organic farms compared to conventional. In addition, when parental provisioning behaviour was not restricted by predation risk (i.e., at times of low corvid activity), nestling provisioning rates were higher at lower territory densities, resulting in a much greater increase in nestling mass in low density areas, suggesting that food limitation occurred at high densities. These findings in turn suggest an ecological trap, whereby preferred nesting habitat does not provide sufficient food for rearing nestlings at high population density, creating a population sink. Habitat management for farmland birds should focus not simply on creating a high nesting density, but also on ensuring heterogeneous habitats to provide food resources in close proximity to nesting birds, even if this occurs through potentially restricting overall nest density but increasing population-level breeding success.

The protozoan parasite Trichomonas gallinae causes adult and nestling mortality in a declining population of European Turtle Doves, Streptopelia turtur.

Studies incorporating the ecology of clinical and sub-clinical disease in wild populations of conservation concern are rare. Here we examine sub-clinical infection by Trichomonas gallinae in a declining population of free-living European Turtle Doves and suggest caseous lesions cause mortality in adults and nestlings through subsequent starvation and/or suffocation. We found a 100% infection rate by T. gallinae in adult and nestling Turtle Doves (n = 25) and observed clinical signs in three adults and four nestlings (28%). Adults with clinical signs displayed no differences in any skeletal measures of size but had a mean 3.7% reduction in wing length, with no overlap compared to those without clinical signs. We also identified T. gallinae as the suggested cause of mortality in one Red-legged Partridge although disease presentation was different. A minimum of four strains of T. gallinae, characterized at the ITS/5.8S/ITS2 ribosomal region, were isolated from Turtle Doves. However, all birds with clinical signs (Turtle Doves and the Red-legged Partridge) carried a single strain of T. gallinae, suggesting that parasite spill over between Columbidae and Galliformes is a possibility that should be further investigated. Overall, we highlight the importance of monitoring populations for sub-clinical infection rather than just clinical disease.

Long-term individual foraging site fidelity--why some gannets don't change their spots.

Many established models of animal foraging assume that individuals are ecologically equivalent. However, it is increasingly recognized that populations may comprise individuals who differ consistently in their diets and foraging behaviors. For example, recent studies have shown that individual foraging site fidelity (IFSF, when individuals consistently forage in only a small part of their population's home range) occurs in some colonial breeders. Short-term IFSF could result from animals using a win-stay, lose-shift foraging strategy. Alternatively, it may be a consequence of individual specialization. Pelagic seabirds are colonial central-place foragers, classically assumed to use flexible foraging strategies to target widely dispersed, spatiotemporally patchy prey. However, tracking has shown that IFSF occurs in many seabirds, although it is not known whether this persists across years. To test for long-term IFSF and to examine alternative hypotheses concerning its cause, we repeatedly tracked 55 Northern Gannets (Morus bassanus) from a large colony in the North Sea within and across three successive breeding seasons. Gannets foraged in neritic waters, predictably structured by tidal mixing and thermal stratification, but subject to stochastic, wind-induced overturning. Both within and across years, coarse to mesoscale (tens of kilometers) IFSF was significant but not absolute, and foraging birds departed the colony in individually consistent directions. Carbon stable isotope ratios in gannet blood tissues were repeatable within years and nitrogen ratios were also repeatable across years, suggesting long-term individual dietary specialization. Individuals were also consistent across years in habitat use with respect to relative sea surface temperature and in some dive metrics, yet none of these factors accounted for IFSF. Moreover, at the scale of weeks, IFSF did not decay over time and the magnitude of IFSF across years was similar to that within years, suggesting that IFSF is not primarily the result of win-stay, lose-shift foraging. Rather, we hypothesize that site familiarity, accrued early in-life, causes IFSF by canalizing subsequent foraging decisions. Evidence from this and other studies suggests that IFSF may be common in colonial central-place foragers, with far-reaching consequences for our attempts to understand and conserve these animals in a rapidly changing environment.

Seabird movement reveals the ecological footprint of fishing vessels.

Exploitation of the seas is currently unsustainable, with increasing demand for marine resources placing intense pressure on the Earth's largest ecosystem [1]. The scale of anthropogenic effects varies from local to entire ocean basins [1-3]. For example, discards of commercial capture fisheries can have both positive and negative impacts on scavengers at the population and community-level [2-6], although this is driven by individual foraging behaviour [3,7]. Currently, we have little understanding of the scale at which individual animals initiate such behaviours. We use the known interaction between fisheries and a wide-ranging seabird, the Northern gannet Morus bassanus[3], to investigate how fishing vessels affect individual birds' behaviours in near real-time. We document the footprint of fishing vessels' (≥15 m length) influence on foraging decisions (≤11 km), and a potential underlying behavioural mechanism, by revealing how birds respond differently to vessels depending on gear type and activity. Such influences have important implications for fisheries, including the proposed discard ban [8]), and wider marine management.

Sustainable management in crop monocultures: the impact of retaining forest on oil palm yield.

Tropical agriculture is expanding rapidly at the expense of forest, driving a global extinction crisis. How to create agricultural landscapes that minimise the clearance of forest and maximise sustainability is thus a key issue. One possibility is protecting natural forest within or adjacent to crop monocultures to harness important ecosystem services provided by biodiversity spill-over that may facilitate production. Yet this contrasts with the conflicting potential that the retention of forest exports dis-services, such as agricultural pests. We focus on oil palm and obtained yields from 499 plantation parcels spanning a total of ≈23,000 ha of oil palm plantation in Sabah, Malaysian Borneo. We investigate the relationship between the extent and proximity of both contiguous and fragmented dipterocarp forest cover and oil palm yield, controlling for variation in oil palm age and for environmental heterogeneity by incorporating proximity to non-native forestry plantations, other oil palm plantations, and large rivers, elevation and soil type in our models. The extent of forest cover and proximity to dipterocarp forest were not significant predictors of oil palm yield. Similarly, proximity to large rivers and other oil palm plantations, as well as soil type had no significant effect. Instead, lower elevation and closer proximity to forestry plantations had significant positive impacts on oil palm yield. These findings suggest that if dipterocarp forests are exporting ecosystem service benefits or ecosystem dis-services, that the net effect on yield is neutral. There is thus no evidence to support arguments that forest should be retained within or adjacent to oil palm monocultures for the provision of ecosystem services that benefit yield. We urge for more nuanced assessments of the impacts of forest and biodiversity on yields in crop monocultures to better understand their role in sustainable agriculture.

Active blood parasite infection is not limited to the breeding season in a declining farmland bird.

Avian blood parasites can have significant impacts on adult breeding birds but studies of parasitism outside the breeding season are rare, despite their potentially important implications for host-parasite dynamics. Here we investigate temporal dynamics of blood parasite infection in adult yellowhammers Emberiza citrinella . We screened blood samples collected between December and April of 2 consecutive winters using PCR. We found a high prevalence of both Haemoproteus and Leucocytozoon parasites, with a mean prevalence of 50% across 2 winters. Prevalence of both parasites was higher during the second, colder winter of the study. Temporal trends differed between the 2 genera, suggesting that chronic Haemoproteus infections gradually disappear throughout the winter but that Leucocytozoon infections exhibit a relapse during late winter, possibly coincident with reduced food availability. Our results highlight the difference in temporal dynamics between 2 blood parasite genera infecting the same host population and emphasize the need for accurate assessment of infection status at appropriate time periods when examining impacts of, and associations with, blood parasite infection. We suggest that further research should investigate the implications of over-winter infection for birds' physiology, behavior, and survival.